A New Interpretation on the Homology of the Teleostean Telencephalon Based on Hodology and a New Eversion Model

Abstract

Various hypotheses regarding the homology of the teleostean telencephalon with that of other vertebrates have been proposed to date. However, a firm conclusion on this issue has yet to be drawn. We propose here a new hypothesis with a new eversion model. Our hodological data and the analysis of dorsal telencephalic organization in adult cyprinids suggest that: (1) the area dorsalis pars posterior corresponds to the lateral pallium; (2) ventral region of area dorsalis pars lateralis to the medial pallium; (3) pars medialis, dorsal region of pars lateralis, pars dorsalis, and pars centralis of the area dorsalis to the dorsal pallium, and (4) nucleus taenia to the ventral pallium. We propose in a three dimensional model that the eversion process occurs not only dorsolaterally but also caudolaterally. We consider that the caudally directed component dominates for ventral zones of the pallium, or the lateral and ventral pallia; and the periventricular surface of these zones shift caudally, laterally, and then rostrally in teleosts with pronounced telencephalic eversion. This new model fits well with the putative homology based on hodology and the organization of telencephalic divisions in the adult brain.

Subdivisions of the adult zebrafish pallium based on molecular marker analysis

“…Being homologous to the lateral pallium, it should be located next to Dm in the embryo, the presumptive ventral pallium. The discrepancy between the position of Dp in the adult and an expected location next to Dm has led to different models to explain the different position of Dp in the adult pallium: “the partial pallial eversion model” by Wullimann and Mueller 31, 32, 52, 74 , the “eversion-rearrangement theory” by Northcutt and Braford 33, 64, 75 , and the “new eversion model” by Yamamoto and colleagues 37 . In the “partial pallial eversion model” 31, 32, 52, 74 , based on connectional and gene expression data, it has been proposed that the homolog of the lateral pallium does not participate in the eversion.…”

“…Yamamoto and colleagues propose that ventral pallial and lateral pallial homologs are not present in the rostral but only in the caudal pallium. In their model they suggest that Dp is homologous to the lateral pallium 37 . In contrast, we find the putative ventral or ventral/lateral pallial homolog Dm contiguously from rostral to caudal.…”

“…In addition, it has been noted that Dc shows no significant immunoreactivity to Calretinin, Neuropeptide Y or Thyrosine hydroxylase separating it from the surrounding areas of the pallium 79 . Other models based mainly on topology suggest that Dm, Dd and Dld are homologous to the dorsal pallium 37 , whereas others have homologized Dd with the dorsal pallium 4, 29, 30, 33, 64 and have suggested that Dc is not a separate unit, but represents the deeper zone of the periventricular areas of Dm, Dd and Dl. Our gene expression data is consistent with the second part of the “modified pallial eversion model” of Mueller and colleagues.…”

Evolution of the forebrain — revisiting the pallium

“…1D), the neocortex does not arise by simple radial migration from a proliferative ependymal layer, but also entails long-distance radial and tangential migrations from basal forebrain areas (Anderson et al, 1997). In fishes too, large-scale migrations of neuronal populations from their site of origin may account for the final appearance of the adult telencephalon (Yamamoto et al, 2007). The realization that a cell group's location in adults with respect to the lateral ventricle may not be related to its function or embryonic site of origin is of fundamental importance when trying to define homologies for parts of non-mammalian and mammalian brains.…”

“…This organization led early comparative anatomists to the view that the telencephalon in teleosts EDITORIAL was entirely subpallial. But as was the case for birds, studies on molecular and hodological features of the forebrain in these fishes have led to the realization that pallial-equivalent cell groups are present despite the location of these groups below the ventricle (Wullimann and Mueller, 2004;Yamamoto et al, 2007;Northcutt, 2006;Nieuwenhuys, 2009;Mueller et al, 2011HarveyGirard et al, 2012Ganz et al, 2012). Recent hodological, neurochemical, and molecular studies suggest that lampreys also possess pallial and subpallial homologues (Murakami et al, 2001;Stephenson-Jones et al, 2012;Sugahara et al, 2013).…”